How a haemosporidian parasite of bats gets around: The genetic structure of a parasite, vector and host compared

Molecular Ecology

Volumn 24, Issue 4, 2015, Pages 926-940

  Witsenburg, F ^a   Clement L ^a   Lopez Baucells A ^b   Palmeirim, J ^c   Pavlinic I ^d   Scaravelli, D ^e   Sevcik M ^f   Dutoit, L ^g   Salamin, N ^a,h   Goudet, J ^a   Christe, P ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b Granollers Museum of Natural Sciences   (Spain)

^c UNIVERSITY OF LISBON   (Portugal)

^d CROATIAN NATURAL HISTORY MUSEUM   (Croatia)

^e UNIVERSITY OF BOLOGNA   (Italy)

^f CHARLES UNIVERSITY   (Czech Republic)

^g UPPSALA UNIVERSITY   (Sweden)

^h SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

Author keywords

co evolution; dispersal; Haemosporida; Nycteribiidae; population genetics; vector transmitted parasite

Indexed keywords

HAEMOSPORIDA; MINIOPTERUS SCHREIBERSII; NYCTERIBIIDAE; STREBLIDAE;

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ANIMAL; ANIMAL DISPERSAL; BAT; DISEASE CARRIER; DNA SEQUENCE; EUROPE; GENE FLOW; GENETICS; HAEMOSPORIDA; HOST PARASITE INTERACTION; MOLECULAR GENETICS; PARASITOLOGY; POPULATION GENETICS;

ANIMAL DISTRIBUTION; ANIMALS; CHIROPTERA; DISEASE VECTORS; DNA, MITOCHONDRIAL; EUROPE; GENE FLOW; GENETICS, POPULATION; HAEMOSPORIDA; HOST-PARASITE INTERACTIONS; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA;

EID: 84923093600     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13071     Document Type: Article

References (55)

1. Bensch S, Stjernman M, Hasselquist D et al. (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society B-Biological Sciences, 267, 1583-1589.
2. Bensch S, Perez-Tris J, Waldenstrom J, Hellgren O (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution, 58, 1617-1621.
3. Blasco-Costa I, Poulin R (2013) Host traits explain the genetic structure of parasites: a meta-analysis. Parasitology, 140, 1316-1322.
4. Bruyndonckx N, Dubey S, Ruedi M, Christe P (2009) Molecular cophylogenetic relationships between European bats and their ectoparasitic mites (Acari, Spinturnicidae). Molecular Phylogenetics and Evolution, 51, 227-237.
5. Bruyndonckx N, Biollaz F, Dubey S, Goudet J, Christe P (2010) Mites as biological tags of their hosts. Molecular Ecology, 19, 2770-2778.
6. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657-1659.
7. Curtis VA (2014) Infection-avoidance behaviour in humans and other animals. Trends in Immunology, 35, 457-464.
8. Dick CW, Patterson BD (2008) An excess of males: skewed sex ratios in bat flies (Diptera: Streblidae). Evolutionary Ecology, 22, 757-769.
9. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software, 22, 1-20.
10. Duval L, Mejean C, Maganga GD et al. (2012) The chiropteran haemosporidian Polychromophilus melanipherus: a worldwide species complex restricted to the family Miniopteridae. Infection, Genetics and Evolution, 12, 1558-1566.
11. Earl DA, Vonholdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359-361.
12. Estrada-Peña A, Serra-Cobo J (1991) The Acarinia and Nycteribidia zones of Miniopterus schreibersii Kuhl (Mammalia: Chiroptera) in the northeast of Spain. Folia Parasitologica, 38, 345-354.
13. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611-2620.
14. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes-application to human mitochondrial-DNA restriction data. Genetics, 131, 479-491.
15. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics, 1, 47-50.
16. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 164, 1567-1587.
17. Fumagalli L, Taberlet P, Favre L, Hausser J (1996) Origin and evolution of homologous repeated sequences in the mitochondrial DNA control region of shrews. Molecular Biology and Evolution, 13, 31-46.
18. Gardner RA, Molyneux DH, Stebbings RE (1987) Studies on the prevalence of Hematozoa of British bats. Mammal Review, 17, 75-80.
19. Garnham PCC (1966) Malaria Parasites and Other Haemosporidia, 1st edn. Blackwell Scientific Publications, Oxford.
20. Gomez-Diaz E, Boulinier T, Sertour N et al. (2011) Genetic structure of marine Borrelia garinii and population admixture with the terrestrial cycle of Lyme borreliosis. Environmental Microbiology, 13, 2453-2467.
21. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www.unil.ch/izea/softwares/fstat.html. Updated from Goudet (1995).
22. Goudet J (2005) HIERFSTAT, a package for R to compute and test hierarchical F-statistics. Molecular Ecology Notes, 5, 184-186.
23. Jarne P, Théron A (2001) Genetic structure in natural populations of flukes and snails: a practical approach and review. Parasitology, 123, S27-S40.
24. Jost L (2008) G(ST) and its relatives do not measure differentiation. Molecular Ecology, 17, 4015-4026.
25. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide-sequences. Journal of Molecular Evolution, 16, 111-120.
26. Lanza B (1999) I parassiti dei pipistrelli (Mammalia, Chiroptera) della fauna italiana. Museo Regionale di Scienze Naturali Torino, Turin.
27. Levin II, Parker PG (2013) Comparative host-parasite population genetic structures: obligate fly ectoparasites on Galapagos seabirds. Parasitology, 140, 1061-1069.
28. Louhi KR, Karvonen A, Rellstab C, Jokela J (2010) Is the population genetic structure of complex life cycle parasites determined by the geographic range of the most motile host? Infection, Genetics and Evolution, 10, 1271-1277.
29. Lourenc¸o S, Palmeirim JM (2008) Which factors regulate the reproduction of ectoparasites of temperate-zone cave-dwelling bats? Parasitology Research, 104, 127-134.
30. Marshall AG (1970) The life cycle of Basilia hispida Theodor 1967 (Diptera: Nycteribiidae) in Malaysia. Parasitology, 61, 1-18.
31. McCoy KD, Boulinier T, Tirard C (2005a) Comparative host-parasite population structures: disentangling prospecting and dispersal in the black-legged kittiwake Rissa tridactyla. Molecular Ecology, 14, 2825-2838.
32. McCoy KD, Chapuis E, Tirard C et al. (2005b) Recurrent evolution of host-specialized races in a globally distributed parasite. Proceedings of the Royal Society B-Biological Sciences, 272, 2389-2395.
33. Megali A, Yannic G, Christe P (2011) Disease in the dark: molecular characterization of Polychromophilus murinus in temperate zone bats revealed a worldwide distribution of this malaria-like disease. Molecular Ecology, 20, 1039-1048.
34. Miller-Butterworth CM, Jacobs DS, Harley EH (2002) Isolation and characterization of highly polymorphic microsatellite loci in Schreibers' long-fingered bat, Miniopterus schreibersii (Chiroptera: Vespertilionidae). Molecular Ecology Notes, 2, 139-141.
35. Nieberding CM, Olivieri I (2007) Parasites: proxies for host genealogy and ecology? Trends in Ecology & Evolution, 22, 156-165.
36. Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics, 26, 419-420.
37. Petersen FT, Meier R, Kutty SN, Wiegmann BM (2007) The phylogeny and evolution of host choice in the Hippoboscoidea (Diptera) as reconstructed using four molecular markers. Molecular Phylogenetics and Evolution, 45, 111-122.
38. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
39. Prugnolle F, Théron A, Pointier JP et al. (2005) Dispersal in a parasitic worm and its two hosts: consequence for local adaptation. Evolution, 59, 296-303.
40. Prugnolle F, Durand P, Jacob K et al. (2008) A comparison of Anopheles gambiae and Plasmodium falciparum genetic structure over space and time. Microbes and Infection, 10, 269-275.
41. R Core Team (2012) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
42. Ramos Pereira MJ, Salgueiro P, Rodrigues L, Coelho MM, Palmeirim JM (2009) Population structure of a cave-dwelling bat, Miniopterus schreibersii: does it reflect history and social organization? Journal of Heredity, 100, 533-544.
43. Reckardt K, Kerth G (2006) The reproductive success of the parasitic bat fly Basilia nana (Diptera: Nycteribiidae) is affected by the low roost fidelity of its host, the Bechstein's bat (Myotis bechsteinii). Parasitology Research, 98, 237-243.
44. Rodrigues L, Palmeirim JM (2008) Migratory behaviour of the Schreiber's bat: when, where and why do cave bats migrate in a Mediterranean region? Journal of Zoology, 274, 116-125.
45. Rodrigues L, Pereira MJR, Rainho A, Palmeirim JM (2010) Behavioural determinants of gene flow in the bat Miniopterus schreibersii. Behavioral Ecology and Sociobiology, 64, 835-843.
46. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics, 145, 1219-1228.
47. Ryberg O (1947) Studies on Bats and Bat Parasites. Bokförlaget Svensk Natur, Stockholm.
48. Tamura K, Peterson D, Peterson N et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731-2739.
49. Theodor O (1957) Parasitic adaptation and host-parasite specificity in the pupiparous Diptera. In: First Symposium on Host Specificity among Parasites of Vertebrates (ed. Mayr E), pp. 50-63. Union Internationale des Sciences Biologiques Série B, Neuchâtel.
50. Theodor O (1967) An Illustrated Catalogue of the Rothschild Collection of Nycteribiidae. British Museum (Natural History), London.
51. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535-538.
52. Waite JL, Henry AR, Adler FR, Clayton DH (2012) Sex-specific effects of an avian malaria parasite on an insect vector: support for the resource limitation hypothesis. Ecology, 93, 2448-2455.
53. Witsenburg F, Schneider F, Christe P (2014) Signs of a vector's adaptive choice: on the evasion of infectious hosts and parasite-induced mortality. Oikos, online early view. doi: 10.1111/oik.01785.
54. Wood R, Weyeneth N, Appleton B (2011) Development and characterisation of 20 microsatellite loci isolated from the large bent-wing bat, Miniopterus schreibersii (Chiroptera: Miniopteridae) and their cross-taxa utility in the family Miniopteridae. Molecular Ecology Resources, 11, 675-685.
55. Wright S (1951) The genetical structure of populations. Annals of Eugenics, 15, 323-354.